Ozone exposure induces metabolic stress and olfactory memory disturbance in honey bees

Human activities, urbanization, and industrialization contribute to pollution that affects climate and air quality. A main atmospheric pollutant, the tropospheric ozone (O₃), can damage living organisms by generating oxidative radicals, causing respiratory problems in humans and reducing yields and growth in plants. Exposure to high concentrations of O₃ can result in oxidative stress in plants and animals, eventually leading to substantial ecological consequences. Plants produce volatile organic compounds (VOCs) emitted in the environment and detected by pollinators (mainly by their antennae), foraging for nutritious resources. Several pollinators, including honey bees, recognize and discriminate flowers through olfactory cues and memory. Exposure to different concentrations of O₃ was shown to alter the emission of floral VOCs by plants as well as their lifetime in the atmosphere, potentially impacting plant-pollinator interactions. In this report, we assessed the impacts of exposure to field-realistic concentrations of O₃ on honey bees' antennal response to floral VOCs, on their olfactory recall and discriminative capacity and on their antioxidant responses. Antennal activity is altered depending on VOCs structure and O₃ concentrations. During the behavioral tests, we first check consistency between olfactory learning rates and memory scores after 15 min. Then bees exposed to 120 and 200 ppb of ozone do not exert specific recall responses with rewarded VOCs 90 min after learning, compared to controls whose specific recall responses were consistent between time points. We also report for the first time in honey bees how the superoxide dismutase enzyme, an antioxidant defense against oxidative stress, saw its enzymatic activity rate decreases after exposure to 80 ppb of ozone. This work tends to demonstrate how hurtful can be the impact of air pollutants upon pollinators themselves and how this type of pollution needs to be addressed in future studies aiming at characterizing plant-insect interactions more accurately.